Light-induced STOMAGEN-mediated stomatal development inArabidopsisleaves

Abstract

The initiation of stomata, microscopic valves in the epidermis of higher plants that control of gas exchange, requires a co-ordinated sequence of asymmetric and symmetric divisions, which is under tight environmental and developmental control. Arabidopsis leaves grown under elevated photosynthetic photon flux density have a higher density of stomata. STOMAGEN encodes an epidermal patterning factor produced in the mesophyll, and our observations indicated that elevated photosynthetic irradiation stimulates STOMAGEN expression. Our analysis of gain and loss of function of STOMAGEN further detailed its function as a positive regulator of stomatal formation on both sides of the leaf, not only in terms of stomatal density across the leaf surface but also in terms of their stomatal index. STOMAGEN function was rate limiting for the light response of the stomatal lineage in the adaxial epidermis. Mutants in pathways that regulate stomatal spacing in the epidermis and have elevated stomatal density, such as stomatal density and distribution (sdd1) and too many mouth alleles, displayed elevated STOMAGEN expression, suggesting that STOMAGEN is either under the direct control of these pathways or is indirectly affected by stomatal patterning, suggestive of a feedback mechanism. These observations support a model in which changes in levels of light irradiation are perceived in the mesophyll and control the production of stomata in the epidermis by mesophyll-produced STOMAGEN, and whereby, conversely, stomatal patterning, either directly or indirectly, influences STOMAGEN levels.

Transcriptional control of cell fate in the stomatal lineage

“…Because EPF2 downregulates SPCH [27*], this elegantly links perception of an environmental cue--relative elevation of [CO 2 ]--to a decrease in stomatal lineage initiation and stomatal density [27*]. The identification of CRSP as a specific regulator of EPF2 suggests that multiple environmental signals could converge on the signaling pathways that regulate SPCH and a spate of recent papers underscore this regulatory convergence: ABA (abscisic acid), previously known to induce stomatal closure, was recently shown to also regulate stomatal density through SPCH regulation [29], osmotic stress leads to reduction of leaf size in a SPCH-dependent manner [30], and STOMAGEN expression is activated by light, thereby providing a mechanism for the oft-observed increase of stomatal numbers in high light [31]. …”

“…Thus far, proteins that directly regulate SPCH transcription (except SPCH itself [31*]) have not been identified, but other forms of gene expression regulation have been found; the locus has high H3K27me3 in samples from seedling tissues suggesting that chromatin marks help repress the locus in mature leaves [33]. In addition, in response to low humidity, DNA methylation at the SPCH locus increases while SPCH expression (and stomatal density) decrease.…”

“…Due to SPCH’s key role at the start of the stomatal lineage, it is perhaps not surprising to learn that SPCH binds to over 8,000 sites in the genome, and thus can serve as a master regulator of stomatal fate [31*]. SPCH binds to roughly one third of the Arabidopsis genes, a number that while high, is consistent with other lineage establishing transcription factors such as MyoD, a master regulator of mammalian myogenesis [38].…”

The Plant Peptidome: An Expanding Repertoire of Structural Features and Biological Functions

“…In contrast, overexpression of EPFL9 (STOMAGEN) results in increased stomatal density and clustering (Hunt et al, 2010). EPFL9 was recently shown to be involved in the light response of the stomatal pathway (Hronková et al, 2015). NMRderived structural information showed that STOMAGEN represents two antiparallel b-strands connected by a loop (Ohki et al, 2011) (Figure 3).…”

Lineage-specific stem cells, signals and asymmetries during stomatal development

“…Indeed, STOMAGEN expression is upregulated by light, which probably contributes to light-regulated increases in stomatal numbers (Fig. 3) (Hronkova et al, 2015). Genetic studies suggest that light signals perceived by phytochromes and cryptochromes are mediated by CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1), then merge into the YDA-canonical stomatal pathways (Fig.…”